IT IS just about the greatest sacrifice possible, and in evolutionary terms it looks like madness. Forgoing reproduction in order to help raise another’s offspring is a supreme act of altruism. It happens routinely in hundreds of ant, bee and wasp species, where sterile workers toil for the benefit of the queen.
For the last 40 years, the evolution of such altruism has been explained by kin selection: the idea that helping your relatives – and therefore helping spread the genes you share with them – outweighs the cost of not having offspring of your own. It’s the genes that matter, not the individuals in which they reside or the groups in which those individuals live. The idea was encapsulated in Richard Dawkins’s pervasive metaphor of the selfish gene.
Now, in a move that has baffled evolutionary biologists worldwide, the father of sociobiology and the world expert on social insects, Edward O. Wilson, says insect altruism and colonial living do not after all require kin selection to evolve (BioScience, vol 58, p 17). Instead, he cheerfully says, it only requires a small “hop”: “One small step for a wasp, one giant leap for hymenoptera.”
Advertisement
Lightly said, but Wilson’s ideas, if proved correct, would have great consequences. Altruistic behaviour was at one time a Darwinian paradox: how could the individual struggle to survive and reproduce favour such a strategy? The solution became known as Hamilton’s rule (see “To die for two brothers”). It explains, for example, why fertile females in many species of bees and wasps cooperate in reproduction instead of nesting alone. It also explains why castes of permanently sterile workers evolved. Or does it?
Wilson, who is at Harvard University, points out that eusocial behaviour (where a mother “queen” is assisted at the nest by non-reproducing offspring) has been discovered in a variety of organisms. Species of aphids, shrimps, beetles, naked mole rats and others have joined the club. They have many ecological traits in common – in particular a large nest that must be defended from parasites or predators – but very different genetic structures. Naked mole rats, for example, have two sets of chromosomes – making them diploid, like us – and reproduce sexually, also just like us. Aphids, on the other hand, form colonies of genetically identical clones. In aphids, therefore, one might expect altruism to be particularly common, but it is not. These and other observations led Wilson to conclude that kin selection was not the decisive factor in the evolution of sterile workers (see “Kin selection: for and against”).
“Aphids form colonies of identical clones, so you might expect altruism to be particularly common, but it is not”
Flexible lifestyle
Eusociality, argues Wilson, emerges from a rare combination of life-history characteristics and pre-adaptations. In particular, it can only evolve after the insect has gone through a phase where it can be flexible in its behavioural choices. For example, females of a solitary wasp species occasionally take the role of either “queen” or “worker” when forced to nest together. If an environmental change or a new mutation then inhibits the dispersal of their offspring, they will be forced to stay at the natal nest. The pre-adaptations enable them to cooperate efficiently. Thus, says Wilson, fully eusocial colonies emerged in one single leap, and went on evolving by means of group selection, because groups that cooperate do better than those that do not.
Wilson’s “flexibility” scenario for the evolution of eusociality in insects is not new. A similar idea was proposed as an alternative to kin selection about 30 years ago by Mary Jane West-Eberhard, now at the Smithsonian Tropical Research Institute in Panama. She, however, no longer sees flexibility as incompatible with kin selection. “In fact, [it] depends on kin selection to work,” she says. “Hamilton’s rule describes the precise switching point when the flexibly responsive females should stay in the groups and express costly worker aid.”
Wilson’s downgrading of kin selection theory, however, goes beyond its role in eusocial evolution. Kin selection “is not wrong, and it is internally consistent, but it is ineffective”, he says. “If you look at the literature of the theory, there are a lot of impressive-looking mathematical models but they scarcely ever come up with a real measure of anything that can be applied to nature.”
Most evolutionary biologists żěè¶ĚĘÓƵ spoke to strongly disagree. “I think he has rather underestimated what kin selection theory has achieved,” says Andrew Bourke of the University of East Anglia, UK.
“We are finding it useful in studying microbes,” says David Queller at Rice University in Houston, Texas. “It turns out that when they are altruistic they are related too. We weren’t too surprised, because that is a prediction of kin selection theory.”
Kin selection theory “makes all kinds of predictions about social behaviour”, adds Francis Ratnieks of the University of Sheffield, UK. Since many of these predictions have been supported, he says, we can be confident in it.
Wilson’s forthcoming book The Superorganism, written with Bert Hölldobler of Arizona State University in Tempe, will further advance the case for eusociality evolving by group selection in a single leap. “It’s essentially a new paradigm,” he says. However, the two theories might turn out to be compatible.
“Sociobiologists used to think that group selection was completely wrong, and some people still think that way,” says Queller, “but a large number of us think that group selection, if you do it correctly, is just alternative language [to kin selection] for describing social evolution.” For more on this, see Dawkins’s thoughts on Wilson’s paper on page 17.
All researchers agree, though, that there is more to social behaviour than just kin selection. To understand social evolution “we have to look at phylogeny, at gene expression, at anatomy, at behaviour, at ecological context”, says James Hunt of North Carolina State University in Raleigh.
In a nod to the “modelling industry” that has sprung up around Hamilton’s rule, Ratnieks concedes that sometimes models were developed in the absence of biological data. “These models almost had a life of their own, with underlying assumptions that in many cases were never verified.”
Most sociobiologists say Wilson’s ideas don’t herald a scientific revolution. “Kin selection theory has always had its detractors,” says Bourke. “Its critics have seen it as too reductionist, too genetical, perhaps even too Dawkinsian, or they just got bored with it because it became so dominant.”
Wilson is not surprised. “Of course they are going to remain critical for a while,” he says. “I am used to taking the heat, and in the past I turned out to be right. If those who defend the standard theory come back in lucid terms and show, point by point, why these hypotheses are already understood, I’ll be glad to concede. But I haven’t seen any evidence yet. Maybe they will now.”
(see “Editorial: Time for revolution in evolution?”)
Evolution – Learn more about the struggle to survive in our comprehensive special report.
Kin selection: for and against
• WILSON SAYS: Many eusocial species share behavioural and ecological traits with ants and bees, but have different family and genetic structures.
“Hamilton’s rule says that relatedness is essential for altruism to evolve. It never said that relatedness ’caused’ altruism. Other preconditions could be important but you couldn’t have those conditions and zero relatedness and get altruism.”
Andrew Bourke, University of East Anglia, UK
• WILSON SAYS: In most eusocial insects, sterile workers are unable to recognise their closest relatives and do not aid them more than unrelated nestmates.
“Theoretical models [based on kin selection theory] have shown that the information cues to allow individual recognition are bound to be removed by selection, particularly in advanced eusocial systems.”
Jacobus Boomsma, University of Copenhagen, Denmark
• WILSON SAYS: In some social wasps and bees, average genetic relatedness between colony members is very low, because unrelated individuals join the nest and cooperate.
“There is nothing that says you can’t have kin selection for altruism with low relatedness. Therefore, it doesn’t shake my faith in kin selection theory. If it did, it would have the same impact from a group selection view point.”
David Queller, Rice University, Houston, Texas
To die for two brothers
The kin selection revolution started in a pub in the mid 1950s. Biologist J. B. S. Haldane was asked if he would give his life to save his brother. A few scribbled calculations later, he provocatively replied that he would only die for at least two brothers, or eight cousins.
Why? Because a gene coding for such altruism can only survive if it leaves enough copies of itself in relatives. Human siblings share on average half of their genes, and cousins one-eighth. Hence, two siblings, or eight cousins equal one self. The concept was published by Haldane in 1955, but was generalised and mathematically formalised by William Hamilton in 1964.
The revolution ignited. Group selection mechanisms, proposed in particular by Vero Wynne-Edwards, no longer appeared to explain altruism. The individual came to be seen as the protagonist of natural selection. Soon the gene took its place. Bodies could be regarded as merely the genes’ way of making more genes, as famously expressed in 1976 by Richard Dawkins’s metaphor of the selfish gene. In two ground-breaking books, The Insect Societies (1971) and Sociobiology (1975), Edward O. Wilson launched a new research programme that promised to explain the social behaviour of all animals under a single unifying theory, with kin selection at its core.
Sociobiologists faced accusations of racism and sexism, because of their then-radical views on human nature. żěè¶ĚĘÓƵs such as Stephen Jay Gould entered the fray, arguing that there was more to evolution and social behaviour than genes maximising their own fitness. Today, the majority of behavioural ecologists, knowingly or not, follow the gene-centred sociobiological approach. Wilson, however, has now changed flag, turning against what he helped create.
